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Asexual Reproduction Strategies and Blooming Potential in Scyphozoa

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Asexual Reproduction Strategies and Blooming Potential in Scyphozoa Vol. 510: 241–253, 2014 MARINE ECOLOGY PROGRESS SERIES Published September 9 doi: 10.3354/meps10798 Mar Ecol Prog Ser Contribution to the Theme Section ‘Jellyfish blooms and ecological interactions’ Asexual reproduction strategies and blooming potential in Scyphozoa Agustín Schiariti1,2,*, André C. Morandini3, Gerhard Jarms4, Renato von Glehn Paes3, Sebastian Franke4, Hermes Mianzan1,2 1Instituto Nacional de Investigación y Desarrollo Pesquero (INIDEP), Paseo V, Ocampo No. 1, B7602HSA Mar del Plata, Argentina 2Instituto de Investigaciones Marinas y Costeras (IIMyC), CONICET, Universidad Nacional de Mar del Plata, 7600 Argentina 3Departamento de Zoologia, Instituto de Biociências, Universidade de São Paulo (USP), Rua do Matão trav. 14 n. 101, São Paulo, 05508-090 SP, Brazil 4Biocenter Grindel and Zoological Museum, University of Hamburg, Martin-Luther-King Platz 3, 20146 Hamburg, Germany ABSTRACT: Scyphistomae show different modes of propagation, occasionally allowing the sudden release of great numbers of medusae through strobilation leading to so-called jellyfish blooms. Accordingly, factors regulating asexual reproduction strategies will control scyphistoma density, which, in turn, may influence blooming potential. We studied 11 scyphistoma species in 6 combinations of temperature and food supply to test the effects of these factors on asexual repro- duction strategies and reproduction rates. Temperature and food availability increased reproduc- tion rates for all species and observed reproduction modes. In all cases, starvation was the most important factor constraining the asexual reproduction of scyphistomae. Differences in scyphis- toma density were found according to the reproductive strategy adopted by each species. Differ- ent Aurelia lineages and Sanderia malayensis presented a multi-mode strategy, developing up to 5 propagation modes. These species reached the highest densities, mostly through lateral budding and stolons. Cassiopea sp., Cephea cephea, Mastigias papua and Phyllorhiza punctata adopted a mono-mode reproductive strategy, developing only free-swimming buds. Lychnorhiza lucerna, Rhizostoma pulmo and Rhopilema esculentum also presented a mono-mode strategy, but they only developed podocysts. These 3 species had the lowest reproduction rates and polyp densities; not only their reproduction rates but also the need for a 2-fold set of environmental stimuli to pro- duce new polyps (one for encystment, another for excystment) made this reproduction mode the slowest of those observed to be utilized for propagation. We conclude that blooms may be defined phylogenetically by the specific asexual modes each species develops, which, in turn, is regulated by environmental conditions. KEY WORDS: Polyp · Scyphistomae · Mono-mode strategy · Multi-mode strategy · Budding · Podocysts Resale or republication not permitted without written consent of the publisher INTRODUCTION strobilation), leading to population pulses that can sometimes result in medu sa outbreaks or the so- A main feature of the majority of blooming called jellyfish blooms (CIESM 2001). Accordingly, scyphozoans is the presence of a benthic polyp it is logical to assume that once strobilation is trig- stage during which several asexual reproduction gered, the greater the number of scyphistomae, the modes are utilized for propagation. In turn, under higher the number of released medusae. Therefore, specific environmental conditions polyps produce factors regulating polyp density will influence the and release great numbers of ephyrae (through formation of medusae blooms. *Corresponding author: [email protected] © Inter-Research 2014 · www.int-res.com 242 Mar Ecol Prog Ser 510: 241–253, 2014 Different environmental factors have been pro- ent asexual reproduction modes have been described posed to influence scyphistoma asexual reproduction for several species, little is known about the impor- and mortality rates. Among them, temperature and tance of each of them in terms of polyp propagation. food availability appear to be the most important To address these questions we performed a series ones for the majority of species (Lucas et al. 2012). In of experiments involving 11 scyphistoma species. general, reproduction rates increase with tempera- These experiments were organized to evaluate the ture and food supply. However, the results available effect of different combinations of temperature and in the literature are conflicting and have hindered food supply on the asexual reproductive strategy of our understanding of reproductive patterns, as made each species. The null hypotheses tested were that evident in the review by Lucas et al. (2012). reproductive strategy, reproduction rates and polyp One of the reasons behind these controversial density did not differ according to species or experi- results may be found in the diversity of asexual mental conditions. reproductive strategies existing among scyphozoans and their interactions with multiple environmental factors. Only a handful of studies have discriminated MATERIALS AND METHODS between the different asexual modes scyphistomae exhibit during propagation (e.g. Han & Uye 2010), Scyphistomae were reared in laboratory cultures with the majority of studies focusing on the formation from specimens collected in their natural environ- of podocysts and ‘buds’. However, non-coronate ment or obtained from artificial fertilization. All spe- scyphozoans multiply through a variety of asexual cies were maintained inside incubators under the reproduction modes (Adler & Jarms 2009). Although temperatures and salinities provided in Table 1. the final product of these propagation modes is in all Scyphistomae were kept in the dark and fed once cases a new polyp, the use of a particular mode, or a weekly with newly hatched Artemia nauplii. Cul- combination of more than one mode, might have eco- tures were maintained in glass or polystyrene dishes logical implications related to blooming potential. (~200 ml) filled with filtered (5 µm) seawater (34 psu). While some species exhibit the potential to display Although Cassiopea sp., Cephea cephea, Mastigias several asexual modes, even simultaneously, others papua and Phyllorhiza punctata polyps usually host only exhibit a few or just one (Adler & Jarms 2009). zooxanthellae in their tissues (which are important Therefore, considering the reproductive strategy to for strobilation), no studies have indicated that dark- be the number and type of asexual reproduction ness influences other types of asexual reproduction modes displayed and the relative importance of each (except for that of Cassiopea andromeda; Hofmann et mode to polyp density, we hypothesize that those al. 1978). species capable of switching their reproductive stra- Combined effects of temperature and food supply tegy in response to environmental fluctuations will were observed separately for 11 scyphozoan species. have a greater blooming potential. Although differ- The experiments included 3 different temperatures Table 1. List of species, and culture and experimental conditions used in the present study. T2: culture conditions prior to the experiment; T1 and T3: T2 − 5ºC and T2 + 5ºC, respectively. HL: Helgoland; JP: Japan; FR: France Species Track culture/origin Culture conditions Experimental conditions Temp. Salinity Temp. (ºC): Salinity (ºC) T1, T2, T3 Aurelia sp.HL Helgoland, Germany 10 34 5, 10, 15 34 Aurelia sp.JP Kagoshima Bay, Japan 20 34 15, 20, 25 34 Aurelia sp.FR Roskoff, France 20 34 15, 20, 25 34 Sanderia malayensis Same as in Adler & Jarms (2009) 20 34 15, 20, 25 34 Cassiopea sp. Cabo Frio, Brazil 20 34 15, 20, 25 34 Cephea cephea Berlin Zoo Aquarium 20 34 15, 20, 25 34 Mastigias papua Berlin Zoo Aquarium 20 34 15, 20, 25 34 Phyllorhiza punctata Berlin Zoo Aquarium 20 34 15, 20, 25 34 Lychnorhiza lucerna San Clemente del Tuyú, Argentina 20 22 15, 20, 25 22 Rhizostoma pulmo Mar Menor, Spain 15 34 10, 15, 20 34 Rhopilema esculentum Kamo Aquarium, Japan 15 34 10, 15, 20 34 Schiariti et al.: Scyphozoan asexual reproduction and blooming potential 243 (maintained by incubators; Table 1) and 2 feeding ied factors because interaction could not be deter- conditions (starvation, feeding ad libitum). Fully mined due to missing data (no polyps or no reproduc- developed scyphistomae showing no external evi- tive products). In these cases, we used a t-test, 1-way dence of reproduction were detached from the stem ANOVA, or the non-parametric Mann-Whitney and cultures and placed in experimental units (glass Kruskal-Wallis tests depending on whether or not dishes containing 150 ml of filtered seawater). Scyp - each data set met the as sumptions. histomae were allowed to reattach and acclimate to the experimental temperatures for 1 wk without food. Dishes were covered by glass plates to avoid eva - RESULTS poration. They were held in the dark, except during observation periods (~30 min observation−1) and Asexual reproduction modes water exchange. Each experimental unit included 1 individual scyphistoma. Three replicates were uti- We observed the following asexual reproduction lized for each combination of temperature and food modes: typical lateral budding (LB), lateral budding supply, accounting for a total of 18 initial polyps per by means of stolons (LBst), ‘Sanderia-type’ budding species. Experimental temperatures were chosen (StyB), reproduction from parts of stolons/stalks (ST), based on species culture conditions (Table 1). typical free-swimming buds/planuloids (FSB), motile Scyphistomae were fed twice
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